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Evolution of the social brain: How social complexity affects individual cognition in ants

Periodic Reporting for period 1 - BrainiAnts (Evolution of the social brain: How social complexity affects individual cognition in ants)

Reporting period: 2015-08-01 to 2017-07-31

How does social complexity shape brain structure, its associated metabolic costs, and the behavioral capability of individual members of a society? The Social Brain Hypothesis (SBH) posits that larger groups require bigger brains to adaptively process social information, while the Expensive Tissue Hypothesis informs of the cost of producing them. Social insects—ants, bees and wasps—live in groups ranging from hundreds to millions of individuals, have miniaturized brains that nevertheless support striking individual cognitive abilities and are renowned for their remarkable collective intelligence and division of labor. SBH would predict bigger brains for bigger groups, but the distributed processing of information by task-specialized workers might relax the cognitive challenges of individual workers, leading to a reduction in brain investment. Additionally, the associated energetic expenses of brain size are not well understood in any clade; animals with relatively bigger brains might have compensatory mechanisms to lower or compensate brain tissue metabolic costs.

Humans form societies also characterized by division of labor and collective intelligence. However, it is difficult to examine how social life influenced our brain evolution because we are a single species and historical analyses are limited to comparison of cranial capacity of fossil forms. Ants, in contrast, are a species-rich clade that shows broad variation in social complexity and body size, enabling phylogenetic and socioecological contrasts. Our research can help identifying general principles of the evolutionary neurobiology of social animals, including us. The ant miniaturized brains can inform about evolutionary trade-offs, and how selection for neural efficient and minimal neuroarchitectures can solve cognitive problems and support social behavior. Research on ants has additional societal benefits, for example, by inspiring computer scientists to develop distributed computing systems, and inexpensive robots exhibiting swarm intelligence.

Our overall objectives are to understand the relationship between brain size, region investment, metabolic costs and individual cognitive abilities of ant workers under different levels of sociality. We examine the effect of distributed information processing in the form of degree of collective foraging, subcaste polymorphism and colony size on the neurobiological, cognitive and behavioral characteristics of ant workers, and also on the energetic investment in functionally specialized brain compartments that underlie behavior. We apply techniques to study collective animal behavior and neurobiological methodologies on ant species varying in social complexity. This integrated approach allows us to analyze the evolutionary relationship between social complexity and brain evolution.
BrainiAnts started on August 1st, 2015 establishing a collaboration between the laboratory of James Traniello (Boston University, USA) and the research team of Martin Giurfa (Research Center for Animal Cognition, France). During her stay at the Traniello lab, the Marie Skłodowska-Curie (MSCA) fellow has received training in neuroanatomical, neurophysiological and computational imaging techniques, scientific writing, statistical analysis, peer review, and grant proposal evaluation. She is analyzing the effect of social complexity on the capabilities individual ants by comparing sister clades varying in their degree of sociality or worker subcastes within the same species.

We have used complementary approaches:
BRAIN STRUCTURE ANALYSIS
We have collected data (brain images) of different ant species and subcastes. The ant brain is a mosaic of regions associated we different functions; we hypothesize that sociality might underlie a differential regional investment.
- Volumetric analysis of sister clades varying in social complexity: We have collected data from three pairs of ant species that share similar ecologies but vary in typical group size and colony organization
- Volumetric analysis in polymorphic species to analyze the effect of morphological division of labor: To find general trends independent of ecological contexts, we studied anatomical differences between subcastes in several species
Methodological innovation: To calculate brain subregion volumes, brain images are typically manually labeled; this is very time consuming and sensitive to human bias. In collaboration with Ignacio Arganda-Carreras (Basque country University,Spain), we have created statistical brain atlases of ant brains that allow not only to have statistical representations of species of interest but also to automatically label samples, reducing time and human bias.
NEUROMODULATION OF SOCIAL BEHAVIOR ANALYSIS
We have studied the neuromodulation patterns of octopamine, dopamine and serotonin in subcastes of species of ants varying in the type of polymorphism (continuous or discrete). We found patterns that seem to be species specific. We have also completed a meta-analysis of the published data of the function of biogenic amines in insects.
BRAIN METABOLIC COST ANALYSIS
In collaboration with James Waters and Marla Tippings (Providence College, USA), we adapted the Seahorse respiration system (Agilent Technologies) to assess metabolic activity of isolated live brains. We have successfully measured metabolic activity from sister clades varying in their degree of sociality, from different subcastes of the same species, and from other species with great variation in brain size. Our preliminary results show that we can maintain isolated live brains for hours and that bigger brains measured to date have lower metabolic activity than expected given their total mass.
BEHAVIORAL ANALYSIS
The MSCA fellow designed a simple behavioral assessment to evaluate the effect of division of labor on individual capabilities; we have measured differences in activity (average velocity normalized by body length) between worker subcastes of two species of the polymorphic ant genus Pheidole. We have found activity differences between subcastes that are consistent between the two species.

Our research results are being disseminated through the publication of peer-reviewed scientific articles in high-quality journals, in national and international conferences and seminars, and through public outreach.
Most of our preliminary results, and others from the Traniello Lab, suggest that worker task ecology is a great influence on ant brain structure. To separate the role of sociality from the rest of the ecological constraints, we need to extend our analysis to more species and to other aspects of ant neurobiology. Thanks to our two methodological innovations, we have now the capacity to do so:
-We have not only developed atlases for individual ant species, but also found that we can accurately use artificial species-hybrid atlases to automatically trace several species of ants. We can work more rapidly and efficiently, with less human bias, gaining new insights into the conservation of brain anatomy patterns in relation to social behavior within and between species
-The new method for quantification of ant brain metabolism allows us now to dissect the role of body and group size, polymorphism, nutrition and any other factor we might imagine, on the metabolic cost and investment of miniaturized brains at different scales
Conceptual summary of the project